Terminal, but not concurrent prism exposure produces perceptual aftereffects in healthy young adults

Neuropsychologia 50 (2012) 2789–2795

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Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia

Terminal, but not concurrent prism exposure produces perceptual aftereffects in healthy young adults Tracey A. Herlihey a,b,n, Sandra E. Black a,b,c,d, Susanne Ferber a,b,c a

University of Toronto, Department of Psychology, 100 St. George Street, Toronto, Ontario, Canada M5S 3G3 Heart and Stroke Foundation of Ontario, Centre for Stroke Recovery, Sunnybrook Health Sciences Centre, 2075 Bayview Avenue, Toronto, Ontario, Canada M4N 3M5 c Rotman Research Institute, 3560 Bathurst Street, Toronto, Ontario, Canada M6A 2E1 d Faculty of Medicine, 1 Kings College Circle, Toronto, Ontario, Canada M5S 1A8 b

a r t i c l e i n f o

abstract

Article history: Received 15 June 2012 Received in revised form 31 July 2012 Accepted 6 August 2012 Available online 17 August 2012

A short period of prism adaptation (PA) has been shown to reduce spatial neglect symptoms. Recent evidence suggests that the positive effects of PA might be restricted to visually guided actions, with PA having little effect on perception. However, the majority of studies have adopted a concurrent exposure technique that fosters the development of a change in felt arm position (proprioceptive straight ahead, PSA). Few studies have used terminal exposure that promotes a change in the perceived visual direction (visual straight ahead, VSA). The positive effects of PA might appear to be primarily action based because studies have adopted an exposure technique that promotes a change in proprioception. Here, we compare the effects of the two exposure types on a perceptual and a manual line bisection task in healthy young adults. Before and after seven minutes of exposure to leftward displacing prisms we measured performance on two line bisection tasks (manual and perceptual) and perceived straight ahead (PSA and VSA). During the exposure period participants made pointing movements while the view of their pointing arm was either (i) restricted to the second half of the pointing movement (concurrent exposure) or (ii) restricted to the final part of the pointing movement (terminal exposure). In line with the previous research, concurrent exposure produced a large shift in PSA and a shift on the manual line bisection task. Interestingly, terminal exposure produced a large shift in VSA and a shift in performance on the perceptual line bisection task. Our results shed light on the underlying mechanisms of prism-induced neglect recovery and help to address an apparent discrepancy within the literature. & 2012 Elsevier Ltd. All rights reserved.

Keywords: Neglect rehabilitation Prism adaptation Perceptual aftereffects Cognitive aftereffects Pseudo-neglect

1. Introduction Prism glasses, in particular rightward displacing wedge prisms, have been used as a rehabilitation tool for treating unilateral neglect for well over a decade (see Redding & Wallace, 2005; Rossetti et al., 1998). The general procedure involves performing a pointing task during a brief period of exposure to laterally displacing prisms. Prior to donning the prisms the participant completes a series of tests that are then performed again once the prisms have been removed. Performance pre- and post-exposure is then compared. Several studies have shown that patients with spatial neglect benefit from only brief exposure times, with improved performance on mental imagery (Rode, Rossetti, & Boisson, 2001), tactile perception (Maravita et al., 2003), postural control (Tilikete et al., 2001) and even wheelchair navigation (Jacquin-Courtois, Rode, Pisella, Boisson, & Rossetti, 2008). There are, however, also reports that the efficacy

n Corresponding author at: University of Toronto, Department of Psychology, 100 St. George Street, Toronto, Ontario, Canada M5S 3G3. Tel.: þ 1 416 978 1539. E-mail addresses: [email protected] (T.A. Herlihey), [email protected] (S.E. Black), [email protected] (S. Ferber).

0028-3932/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neuropsychologia.2012.08.009

of prism adaptation (PA) in the rehabilitation of neglect may be limited (Ferber, Danckert, Joanisse, Goltz, & Goodale, 2003; Turton, O’Leary, Gabb, Woodward, & Gilchrist, 2010). In a recent review, Striemer and Danckert (2010a) proposed that PA has ameliorative effects only on visually guided action, leaving perceptual aspects of neglect unchanged. Evidence for this distinction between the effects of PA on the recovery of action vs. perceptual components of the neglect syndrome comes from research investigating performance on the manual and perceptual (or landmark) line bisection tasks (Striemer & Danckert, 2010b). For example, it has repeatedly been shown that patient performance on the manual line bisection task, when patients are required to manually mark the centre of a line using a pencil, has improved: that is, following a period of PA the rightward bias was reduced (Farne et al., 2002; Fortis et al., 2010; Nijboer, Nys, van der Smagt, van der Stigchel, & Dijkerman, 2011; Rossetti et al., 1998). The landmark task is the perceptual equivalent of the manual task: the patient is presented with a line that is already bisected and is required to verbally indicate which end of the line is longer or shorter, or which end of the line is closest to, or furthest from the bisector. Unlike performance on the manual line bisection task, which

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requires the patient to make an action, evidence suggests that PA has no effect on the landmark task performance (Striemer & Danckert, 2010b, although see Colent, Pisella, Bernieri, Rode, & Rossetti, 2000). We argue here, however, that instead of focusing solely on the dependent variable, that is, measures of how performance on neglect tests changes after PA, it may be equally important to pay close attention to the independent variable: how prism adaptation is achieved in the first place. When exposing patients to prisms the majority of studies use the procedure originally adopted by Rossetti and colleagues in their seminal paper (Rossetti et al., 1998). This procedure is akin to the ‘‘concurrent’’ exposure technique described by Redding and Wallace (1988) and used extensively in the PA literature. During concurrent exposure an observer can see their arm from at least the elbow to the finger tip (or even the entire arm) during the pointing movement. This type of exposure technique has been shown to promote a particular type of adaptation within the perceptual-motor control loop, namely ‘‘proprioceptive’’ adaptation—a change in the perceived position of the arm relative to the head. In contrast, a second exposure technique, ‘‘terminal’’ exposure, has been shown to promote ‘‘visual’’ adaptation—a change in the perceived position of the eyes relative to the head. During terminal exposure, the observer only has access to their terminal error while pointing; that is, the full arm movement is occluded and only the tip of the finger at the end of the pointing movement is visible. According to the directionality-of-guidance hypothesis proposed by Redding, Clark and Wallace (1985), adaptation occurs in the modality that is being ‘guided’. During concurrent exposure, the observer can visually direct their arm to point accurately at a target. As a result, realignment occurs predominantly in the ‘‘guided’’ proprioceptive system. In contrast, during terminal exposure, the observer does not have access to visual information during the pointing movement (they only see their tip of their finger at the end of the pointing movement) and thus must use proprioceptive information to direct their arm to the perceived target position. In this case, adaptation takes place in the ‘‘guided’’ visual system. So, how is this related to the action vs. perception debate with regards to neglect recovery? Currently, the majority of studies investigating PA as a potential rehabilitation tool utilize the concurrent exposure technique, a technique that primarily promotes proprioceptive adaptation (a change in felt arm position). It is thus unsurprising that when testing for generalized aftereffects, changes are found on tasks that predominantly rely on the action system (e.g., the manual line bisection) and not on tasks that require a perceptual response. We propose that terminal exposure, a technique that promotes visual adaptation, may be more likely to produce perceptual aftereffects. We tested this hypothesis using a sample of healthy young adults. Based on the results of Redding and Wallace (1988) and the directionality-of-guidance hypothesis (Redding et al., 1985), we predicted that the concurrent exposure condition would produce a larger shift in proprioceptive straight ahead (PSA) and, as a result a larger shift on the manual line bisection task. In contrast, we predicted that the terminal exposure condition would produce a larger shift in visual straight ahead (VSA) and, unlike what has been found before, a change in performance on the perceptual line bisection task.

2. Method 2.1. Participants Participants were 20 right-handed undergraduate students (mean age: 21.7 years; 6 males) at the University of Toronto who participated in return for course credit. All participants had normal or corrected to normal vision with contact lenses only. The Ethics Review Board of the University of Toronto approved the study.

Fig. 1. The prism adaptation (PA) box. (A) Rack used to insert the shelf for the terminal adaptation condition; (B) movable light box used for estimating straight ahead; and (C) three targets. 2.2. Materials and procedure Participants performed two line bisection tasks (manual and perceptual) and provided two estimates of perceived straight ahead (visual and proprioceptive) both before and after a period of exposure to wedge prisms displacing the visual image by 101. We chose to use leftward displacing prisms because research in healthy controls suggests that only leftward displacing prisms produce cognitive aftereffects (e.g., Bultitude & Woods, 2010). All participants took part in both a terminal exposure session and a concurrent exposure session across two days of testing (approximately two days apart). For all tasks, participants were seated in front of a PA box with their chin secured in a chin rest. The box allowed measurements of finger movement endpoints with 11 accuracy. The PA box is shown in Fig. 1.

2.2.1. Exposure conditions All participants took part in two exposure conditions across two different test sessions. The order of conditions was random across participants. The concurrent condition, in line with the majority of patient PA studies (e.g., Rossetti et al., 1998), allowed partial sight of the arm (from the elbow and beyond) while pointing (the start of the pointing movement was occluded by the chin rest). For the terminal condition, a shelf was inserted into the PA box and adjusted to restrict view of the pointing movement to the tip of the finger only when the arm was fully extended (see Fig. 1A). For both exposure conditions, while wearing the glasses, participants pointed to three targets in a random order as instructed verbally by the experimenter (one 121 to the left; one 121 to the right; one straight ahead). All targets were positioned at a distance of 86 cm from the observer whose head was secured in a chin rest. Targets were positioned on a semi-circular bar placed at approximately nose level (see Fig. 1C). The target string hung from the bar to below the table. For all pointing movements, when participants extended their arm to point at a target, they were required to place their index finger on the base of the PA box. This helped to reduce fatigue during the exposure period. The timing of pointing was constrained by a metronome set to tick every second.1 Participants were instructed to point in time with the metronome so that their arm was fully extended on the first tick and then placed back on the starting position on the second tick. The starting position was a piece of black textured fabric stuck to the base of the PA box, 6 cm in front of the chin rest, secured to the desk. Participants were given time to practice this procedure prior to donning the prisms. During prism exposure participants made a total of 204 pointing movements, pointing 68 times to each of the three targets (pointing order was randomized prior to the participant arriving at the lab). Total exposure time was 6 min and 48 s.

2.2.2. Measuring straight ahead We used standard measures of perceived straight ahead (proprioceptive and visual, see Redding and Wallace, 1997).2 For both measures participants were seated with their head secured in a chin rest. Measures were completed in a

1 While evidence suggests that the one second pointing rate favors a shift in proprioceptive straight ahead even with terminal feedback (see Redding & Wallace, 1992, 1994) we chose this timing here to remain consistent with the previous research (e.g., Bultitude & Woods, 2010). 2 A third ‘‘Total Shift’’ measure, which we did not take here, is sometimes taken as an additivity check on the purity of the proprioceptive and visual measures of straight ahead (Redding & Wallace, 2006).

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3.5

Concurrent Terminal

3 Change in perceived direction (°)

random order and were repeated six times both before and after exposure to the prisms. For proprioceptive straight-ahead (PSA), participants began by placing their right index finger on the starting position. With eyes closed participants were required to extend and guide their arm so that it was pointing straight ahead of their body. Once the participant was happy with their estimate, the experimenter marked the response on tape attached to the back of the PA box. The participant was then instructed to return their index finger to the starting position ready to point again. Since this task was performed in the absence of any visual feedback, any changes from pre- to post-prism exposure are thought to be the result of a realignment of felt arm (head-hand) position. Visual straight ahead (VSA) was measured in darkness. The experimenter moved a single light attached to the top of the semi-circular bar at the far end of the PA box at approximately eye height. The semi-circular bar was used to ensure that the light remained at the same distance (86 cm) from the participant at all times while moving. The participant’s task was to verbally indicate when the light appeared to be straight ahead. The experimenter then recorded the response by making a mark on a piece of tape attached to the metal bar. The light was moved from both the left and right side of space in a random order. Change in the task performance from pre- to post-exposure is thought to indicate change in perceived eye-head position (Hay & Pick, 1966).

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2.5 2 1.5 1 0.5 0 −0.5 PSA

2.2.3. Line bisection tasks Both line bisection tasks were programmed to run on a Motorola XOOMs tablet (screen size 10.1 in., diagonal). For both tasks, a white horizontal line (187 mm) was presented in the centre of the screen. The tablet was placed at eye level on a shelf inserted inside the PA box approximately 20 cm from the participant. Participants performed both line bisection tasks without prisms, before and after a period of adaptation. Changes from pre- to post-exposure were taken as an indication of adaptation. For the manual line bisection (MLB), participants used a stylus held in their right hand to indicate the centre of the line; the response was displayed on the screen in red. After each response, there was a 500 ms delay before the response was removed from the screen and the line was masked by a random array of coloured squares (covering an area of between 188  9 mm and 204  25 mm on the screen). The mask was presented for 1000 ms followed by a blank screen for 1000 ms before the next line was presented. After making each response, participants were required to move their hand away from the screen before going on to make their next response. Ten lines were presented in total. The perceptual line bisection (PLB) task was similar to the pen and paper task used by Striemer and Danckert (2010b). Sixteen lines were used in total. Each white horizontal line was bisected with a red vertical line (height¼ 10 mm). For 6 of the 16 lines, the bisector appeared randomly 1, 2, or 3 mm to the left or right of centre. For the remaining 10 lines, the bisector appeared in the centre. Only trials in which the bisector appeared in the centre were used for analysis. Each trial began with an instruction screen specifying whether the participant had to indicate which end of the upcoming bisected line was longer, or which end of the line was shorter. The experimenter tapped the screen for the trial to continue. The bisected line was then immediately presented. Each line was presented for 500 ms followed by a mask of coloured squares until response. Participants were to respond verbally saying out loud either ‘‘left’’ or ‘‘right’’. The experimenter tapped the screen to reveal a response box and then entered the participant’s verbal response accordingly. Lines were presented in a random order and participants were informed that no bisector line appeared in the centre of the screen. Task ‘types’ (i.e., line bisection or straight ahead) were performed in pairs, for example, the participant performed the MLB and PLB in succession before performing the two straight ahead tasks or vice versa. However, ‘type’ order (i.e., MLB vs. PLB, PSA vs. VSA) was counterbalanced across participants.

3. Results 3.1. Straight-ahead judgments Change in perceived PSA and VSA from before to after prism exposure is shown in degrees of visual angle in Fig. 2. Adaptation in the correct direction (i.e., to the left for VSA and to the right for PSA)3 was assigned a positive value. A repeated measures ANOVA 3 When wearing leftward displacing prisms a participant will initially make errors to the left of the target. After a period of adaptation the participant will start to point to the right to compensate for their leftward error. Due to realignment, the hand feels to be to the right of its true position. Thus when asked to point straight ahead without vision the observer will point to the right. With regards to visual adaptation, using leftward displacing prisms, perceived visual direction is displaced to the left, causing the eyes (or head) to feel straight ahead when they are actually turned to the left. Thus, when participants are asked to position a visual target to be straight ahead of them, they will position it as being to the left.

VSA

Fig. 2. Mean change in perceived proprioceptive straight ahead (PSA) and visual straight ahead (PSA) as a function of exposure type. Positive values indicate change in the adaptive direction. Error bars represent standard error (SE).

with two factors (Measure: PSA, VSA and Exposure Type: terminal, concurrent) revealed a significant main effect of Measure [F(1, 19)¼ 4.827, p ¼0.041] indicating that in both the terminal and concurrent conditions PSA shift was significantly greater than VSA shift. Although the main effect of Exposure Type was not found to be significant (p¼0.973), the interaction between Measure and Exposure approached significance [F(1, 19) ¼30.628, p ¼0.071] suggesting that the magnitude of PSA and VSA shift varied as a function of Exposure Type. Paired one-tailed t-tests conducted on PSA and VSA separately found a significant difference between the magnitude of VSA in the concurrent and terminal conditions [t(19)¼ 1.963, p ¼0.028], but no significant difference in the magnitude of PSA as a function of Exposure Type (p ¼0.118). 3.2. Line bisection results Unlike what has been found before (e.g., see Jewell & McCourt, 2000 for a review of pseudo-neglect), we were unable to replicate pseudo-neglect (a pre-existing leftward bias prior to exposure to the prisms) in our sample for the MLB task. Indeed, across both exposure conditions pre-PA bisections were slightly to the right of centre (0.54 mm or 0.55%); however, this slight bias was not found to be significant. For the PLB task, the percentage of ‘‘left’’ and ‘‘right’’ responses were calculated for the 10 lines on which the vertical bisector was positioned in the centre of the horizontal line. Lines were split according to the type of response made (i.e., whether the participants had to indicate which end of the line was longer or shorter). A rightward bias would correspond to participants making more ‘‘right’’ responses when asked to indicate which end of the line was the shortest, and more ‘‘left’’ responses when asked to indicate which end of the line was longest. A leftward bias would correspond to the participant making more ‘‘left’’ responses when asked to indicate which end of the line was shortest, and more ‘‘right’’ responses when asked to indicate which end of the line was longest. Prior to exposure to the prisms, responses indicated a slight, albeit non-significant leftward bias. Across both test sessions, approximately 52.8% of responses were made in favour of perceiving the bisector to be slightly to the left of the centre of the line prior to exposure to the prisms. Change in performance on the MLB and PLB tasks after exposure to leftward displacing prisms is shown in Fig. 3.

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0.8

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−0.08 Concurrent

Terminal

MLB

Concurrent

Terminal

PLB

Fig. 3. Mean change in performance from before to after prism adaptation on the manual line bisection task (MLB) and perceptual line bisection task (PLB) as a function of exposure type. Positive values indicate a shift to the right. Error bars represent standard error (SE).

Visual inspection of Fig. 3 suggests a rightward shift in the MLB performance only after concurrent exposure. In contrast, the data suggests a rightward shift in the PLB performance only after terminal exposure. This fits with the predictions outlined in the introduction. However, these trends were not found to be significant using paired two-tailed t-tests (PSA, t(19) ¼0.462, p ¼ 0.649; VSA, t(19) ¼ 0.443, p ¼0.663).

3.2.1. Line bisection and pseudo-neglect The lack of significant effects in Fig. 3 could potentially be explained by the lack of pseudo-neglect demonstrated in the preadaptation measures. Evidence suggests that cognitive aftereffects only occur on tasks where a bias already exists. For example, it is usually found that healthy controls exhibit a small leftward bias on the MLB task that is shifted to the right after PA (e.g., Berberovic & Mattingley, 2003; Colent et al., 2000; Striemer & Danckert, 2010b). Prism adaptation has also been shown to influence the performance on other tasks on which healthy participants generally tend to exhibit a bias, for example, the mental number line (Nicholls, Kamer, & Loftus, 2008), hierarchical figures (Bultitude and Woods, 2010), and the greyscales task (Loftus, Vijayakumar, & Nicholls, 2009). Here, when taking a mean of all participants’ performance, we did not find any evidence for pseudo-neglect, particularly on the MLB task. This is inconsistent with the previous results. One could hypothesize that if we looked only at the participants who demonstrated pseudo-neglect the trend shown in Fig. 3 would be significant. But first it is important to know if a leftward bias on the MLB and PLB is consistent across the two testing sessions, that is, is it a consistent trait within an individual? A Pearson product–moment correlation revealed a significant positive relationship between PLB performance on sessions 1 and 2 [r ¼0.615, p ¼0.004] and a result that approached significance for MLB [r ¼0.420, p¼ 0.066]. These findings provide a good indication that the pre-existing bias participants brought to the laboratory on session 1 were consistent across testing sessions. We thus went ahead and split the participants according to whether they had a leftward or rightward bias on the preexposure MLB and PLB tasks. When selecting participants based on a pre-existing bias we noticed that exhibiting a bias on the MLB task did not necessitate

a bias on the PLB task and vice versa. Indeed, a Pearson product– moment correlation did not reveal a significant relationship between MLB bias and PLB bias both on session 1 [r ¼  0.273; p¼0.244] and session 2 [r ¼  0.265; p ¼0.259]. Of the 20 participants that took part in the experiment, 11 demonstrated a leftward bias on the MLB task and 11 demonstrated a leftward bias on the PLB task, of these participants 5 had a leftward bias on both tasks. Mean pre-exposure MLB bias for this group of 11 participants was 0.8 mm (0.9%) to the left of the centre prior to prism exposure. The mean pre-exposure PLB bias was 69% in favour of perceiving the bisector line to be to the left prior to prism exposure. Data for these selected participants are shown in Fig. 4. The trend presented in Fig. 3 for all participants is much more pronounced in Fig. 4 when looking solely at participants who exhibited a pre-adaptation leftward bias (pseudo-neglect). In line with our original predictions, the shift in performance on the MLB task is significantly larger after concurrent exposure compared to terminal exposure [t(19)¼3.402, p ¼0.007]. Change in the MLB performance after terminal exposure is not significantly different from zero [t(10) ¼  1.056, p¼0.316]. The shift in performance on the PLB task is significantly larger after terminal exposure compared to concurrent exposure [t(19) ¼  2.809, p ¼0.019]. Change in the PLB performance after concurrent exposure is not significantly different from zero [t(10)¼  0.922, p¼0.378]. Combined, the results suggest that using a concurrent exposure technique, which primarily promotes a shift in felt arm position (PSA), leads to a significant rightward shift in performance on a manual and not a perceptual line bisection task. This is in line with the previous research (e.g. Striemer & Danckert, 2010b). The most important finding comes from the terminal exposure condition. Terminal exposure primarily promotes a shift in perceived VSA. Here, we have demonstrated that terminal exposure produces a significant rightward shift only on a perceptual and not a manual line bisection task. Intuitively, this finding would lead one to predict a significant relationship between the magnitude of PSA and MLB shift, and between VSA and PLB shift. Interestingly however, this was not the case; we did not find any significant relationships between shifts in perceived straight ahead and shifts on the line bisection tasks (see Table 1).

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0.6 0.4 0.2 0 −0.2 −0.4

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Concurrent Terminal MLB

Concurrent Terminal PLB

Fig. 4. Results for selected participants demonstrating a leftward pre-adaptation bias (pseudo-neglect) on the MLB (n¼11) and PLB (n¼ 11). Mean change in the performance on the manual line bisection (MLB) and perceptual line bisection (PLB) is shown as a function of exposure type. Positive values indicate a shift to the right. Error bars represent standard error (SE).

T.A. Herlihey et al. / Neuropsychologia 50 (2012) 2789–2795

Table 1 Pearson product moment correlations between the two measure types (straight ahead and line bisection) and the two exposure types (concurrent and terminal). SA, straight ahead; LB, line bisection. Exposure type

SA

LB

r

p

Concurrent Concurrent Terminal Terminal Concurrent Concurrent Terminal Terminal

PSA PSA PSA PSA VSA VSA VSA VSA

MLB PLB MLB PLB MLB PLB MLB PLB

 0.434  0.095  0.187 0.016 0.218 0.029 0.097 0.112

0.857 0.690 0.431 0.946 0.355 0.902 0.685 0.637

4. Discussion The purpose of this study was to address a debate regarding the impact of PA within the realm of neglect rehabilitation. In a sample of healthy young adults, we examined the effect of PA on both a perceptual and a manual line bisection task. We proposed that, in line with the previous research (e.g. Striemer and Danckert, 2010b), an exposure technique used to promote a change in felt arm position (proprioceptive adaptation) would produce a change on a manual line bisection task and no change on a perceptual line bisection task. Indeed, this is what we found – but only for those participants who had a pre-existing leftward bias (pseudo-neglect) on the MLB task. This replicates the previous work demonstrating that PA produces cognitive aftereffects only in participants who exhibit a pre-existing bias (e.g., Bultitude and Woods, 2010; Goedert, Leblanc, Tsai, & Barrett, 2010). The novel result to emerge from this study is the change in performance on the perceptual line bisection task. Previous studies have struggled to demonstrate a shift in perceptual performance post-PA in patients and in healthy controls (Ferber and Danckert, 2006; Striemer and Danckert, 2010b) with one exception (Colent et al., 2000, using a sample of healthy controls only). We proposed that this could be a result of the exposure technique used: many studies adopt a concurrent technique that primarily produces a shift in felt arm position and not a terminal technique that promotes realignment of perceived visual straight ahead. Here, using terminal exposure, we found a substantial change (14.6%) in performance on a perceptual line bisection task after terminal exposure and no change (0.05%) after concurrent exposure. Again, this was only in those participants who exhibited a leftward bias on the PLB task prior to exposure to the prisms. These results demonstrate that one can obtain different types of ‘cognitive’ aftereffects as a function of the exposure technique used—but only when a bias already existed (i.e., the effects were only evident in those showing pseudo-neglect prior to exposure to the prisms). The choice to focus our analysis on participants exhibiting pseudo-neglect was based on evidence suggesting that PA is more likely to influence cognitive functions for which a bias already exists (see Bultitude & Woods, 2010). Unsurprisingly changes in motor performance occur when participants experience a shift in the perceived position of their arm relative to their head. In line with our predictions, we were also able to obtain perceptual changes, but only when participants’ view of their arm was restricted to the tip of their finger during prism exposure, an exposure technique that promotes a shift in perceived VSA. Interestingly, however, although a shift in perceived PSA and VSA appears to be tied to a shift in motor and perceptual performance, respectively, the two were not found to be related: the magnitude of shift in perceived straight ahead was not found to predict the shift in performance on the line bisection tasks. This

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result suggests that it is not realignment magnitude per se that produces cognitive aftereffects, but rather something about the exposure techniques that produces cognitive shifts of attention.4 An aspect of the data that lends itself to this hypothesis is the direction of the aftereffects found for VSA and PLB shift. Although adaptation occurs in different directions for the two measures, when reporting adaptation results authors use the term ‘adaptive direction’, and flip the sign of one of their measures, assigning adaptation that occurred in the correct direction a positive value. Here, we found a rightward shift in PSA, and a rightward shift in the MLB performance after concurrent exposure. After terminal exposure we found a similar rightward shift in the PLB performance, however, VSA shifted to the left. Thus, shift on line bisection performance was not only unrelated to aftereffect magnitude it was also unrelated to the aftereffect direction. Striemer and Danckert (2010b) used concurrent exposure and the MLB and PLB tasks. For both tasks, participants exhibited a pre-adaptation leftward bias. After adaptation, only performance on the MLB task shifted to the right. There was a trend for performance on the PLB task to shift even further to the left, but this was not found to be significant. This result fits nicely with ours. Having a pre-existing bias is not sufficient for a shift in performance to occur. The bias must be matched to the correct exposure technique, or at least the correct type of adaptation must develop for a change to occur. In the case of Striemer and Danckert’s study, only PSA was measured and this was found to be substantial (6.91 of a 101 displacement, compared to 2.81 in our experiment). Since realignment rarely reflects 100% of the induced displacement (e.g., Held & Bossom, 1961), it is thus unlikely that there was a shift in VSA (although since VSA was not measured we cannot be certain of this). An interesting contrast to Striemer’s and our results are those of Colent et al. (2000). Also using concurrent exposure and similar MLB and PLB tasks, Colent et al. found a significant change on PLB, but not MLB, after exposure to leftward displacing prisms in a group of healthy young adults. No effects were found after exposure to rightward displacing prisms. Adaptation was measured using an open loop pointing procedure, which is akin to measuring total shift (combined PSA and VSA). A possible explanation for the lack of change in performance on the MLB task could be a result of the lack of pseudo-neglect—participants manual line bisections were effectively at zero pre-adaptation. There was, however, a pre-adaptation leftward bias on the PLB task. Although Colent et al. did not measure VSA and PSA separately, and concurrent exposure primarily promotes a shift in PSA, it is possible that a shift in VSA did occur. Evidence suggests that given longer exposure times shifts in VSA are not uncommon under concurrent exposure conditions (e.g., Redding & Wallace, 1985). Colent et al. exposed participants to prisms for 20 min, this is substantially longer that that used here (approximately 7 min) and double that used by Striemer (10 min). It is thus possible that the magnitude of visual adaptation was larger in Colent’s experiment than in Striemer’s due to the longer exposure time, and as such produced a shift in the PLB performance as a result. To our knowledge, only one study has contrasted terminal and concurrent exposure directly in patients with neglect (Ladavas, Bonifazi, & Catena, 2011). An interesting finding to emerge from

4 We also tested error reduction from the first six to the last six pointing movements during exposure. In both exposure conditions, all participants pointed accurately towards the targets at the end of adaptation; however, initial error was much larger in the terminal exposure condition compared to the concurrent exposure condition (a result of online correction of pointing in the concurrent condition). As a result, error reduction was much larger in the terminal condition; however, error reduction in both conditions was not related to line bisection shift.

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Ladavas’s study was that the amelioration of perceptuo-motor and oculomotor aspects of neglect was much larger in the terminal exposure group compared to the concurrent exposure group (after an exposure period of 20 min). The authors suggest a possible mechanism for this could be the oculomotor realignment that occurs as a result of the emphasis placed on eye-head coordinates during terminal exposure. However, since this study used an open-loop pointing method to measure adaptation, similar to that used by Colent et al., it is difficult to distinguish the different contributions of a shift in VSA and PSA to the positive aftereffects found. In a similar study, Fortis et al. (2010) tested ‘ecological’ exposure and terminal exposure in patients with neglect, also using an exposure period of 20 min. During ‘ecological’ adaptation participants were required to do a number of different tasks while wearing rightward displacing prisms. Tasks included collecting coins, opening and closing jars, and assembling jigsaw puzzles. Adaptation was measured using a blind pointing procedure similar to the combined PSA and VSA, open loop pointing task used by Colent et al. (2000). Neglect amelioration was measured using a number of different clinical and ecological assessments, including the manual line bisection task and the Catherine Bergego Scale (a measure of performance on activities of daily living, e.g., colliding with objects on the left/right side of space). The authors reported no significant differences between the two groups: the magnitude of pointing aftereffects and the amelioration of neglect were comparable. One major important difference between the two procedures was that patients preferred the ecological activities to the repetitive and fatiguing terminal pointing technique. This is an important consideration to make when deciding which exposure technique to use—given that they produce the same outcome one might suggest using the ecological technique over the terminal technique. However, since the authors did not distinguish between VSA and PSA in their aftereffect measures it is difficult to determine the contribution of these two types of adaptation to the ameliorative effects demonstrated. The dissociation between what we have termed ‘‘visually guided action’’ and ‘‘perception’’ is not the only dissociation with regards to PA efficacy in the neglect rehabilitation literature. In their comprehensive review of the literature, Newport and Schenk (2012) discuss the effect of PA on implicit and explicit perceptual tasks; that is, it appears that PA has an ameliorative effect on tasks that require an explicit perceptual discrimination (e.g., is this face chimeric or non-chimeric, see Sarri, Greenwood, & Kalra, 2011), but not on tasks that require a preference judgment (e.g., ‘‘which side of the face is happy?’’ see Ferber et al., 2003; Sarri, Kalra, Greenwood, & Driver, 2006). While this cannot account for the dissociation between perception and action found here, Newport and Schenk (2012) do offer an interesting alternative explanation (see also Striemer & Danckert, 2010a): they suggest that PA might ameliorate action and not perceptual based components of the neglect syndrome only in patients with a specific pathology (specifically those with lesions to the inferior parietal lobule and the superior temporal gyrus). Although currently there is little empirical support for this claim and it cannot account for the dissociation we have found here in our sample of healthy controls, it does highlight the complexity of PA as a tool for rehabilitating neglect.

5. Conclusion The present study demonstrates that aftereffect type depends crucially on the exposure method used, or at least on the type of aftereffects obtained. These results may help to reconcile some of

the contradictory findings within the PA and neglect literature – although the effects evident in the injured brain are likely to be more exaggerated (e.g., compare Bultitude, Rafal, & List, 2008 with Bultitude & Woods, 2010) – and further build on the literature concerning cognitive aftereffects in healthy participants. Our results stress the importance of measuring both proprioceptive and visual adaptation: using an open loop target pointing task masks the contributions of realignment within these two distinct perceptuo-motor systems (i.e., eye-head and head-hand). Our review of the literature suggests that although exposure technique might play an important role, in particular evidence champions terminal (or ecological) exposure over concurrent, the type of adaptation obtained (i.e., either VSA or PSA) may be more important. Future research should aim to delineate the contributions of VSA and PSA shift to the amelioration of neglect symptoms and should strive to develop an optimal exposure method, and optimal exposure duration.

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